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Representative terms from entire chapter:
carbon gain
NUTRIENT-USE EFFICIENCY AS AN INDICATOR OF
STRESS EFFECTS IN FOREST TREES
R. J. Luxmoore
Environmental Sciences Division
Oak Ridge National Laboratory
Oak Ridge, Tennessee 37831-6038
ABSTRACT
The ratio of plant dry weight gain to total nutrient uptake
provides a lumped whole plant estimate of nutrient use efficiency
(NUE), the net carbon fixed per unit of nutrient uptake. This is
not a practical indicator for whole trees even if the measurement
could be interpreted mechanistically. NUE is difficult to interpret
since the seasonality of nutrient uptake and carbon gain may not
directly coincide, and the internal supply and demand for carbon
and nutrients is buffered by internal storage and matched in
growth through mobilization and internal transport. Sampling of
plant tissues (leaf, fine root) and solutions (phloem, xylem) for
determination
but provides
sampling may
stress effects
knowledge of
tree physiology and phonology. The use of nutrient use
efficiency as an indicator of stress is not practical on a whole
plant basis and is not definitive on a tissue basis at our present
state of knowledge.
of the carbon and nutrient relationships is feasible
fragmented information. Frequent tissue or solution
nevertheless lead to a reliable basis for interpreting
on trees, but this approach requires intimate
the diurnal, wetting and drying, and annual cycles of
The ratio of dry weight gain to net nutrient uptake is one definition of nutrient-
use efficiency (NUE). Another definition is given by the ratio of dry weight gain to
nutrient content and for some tissues such as leaves, NUE is the reciprocal of nutrient
concentration since leaf dry weight is the dry weight gain, and the nutrient content is
the net nutrient uptake. Consideration of the utility of nutrient-use efficiency as an
indicator of stress effects requires evaluation of stress effects on the relative dynamics
of carbon gain and nutrient acquisition. A hyperbolic function (Fig. 1 ) describes the
expected relationship between carbon gain and nutrient uptake up to the maximum carbon
gain (M), where the increment in carbon gain (^C) per increment of nutrient uptake
CONS is zero. The optimum carbon gain (O) is defined as the point at which the second
derivative of the function is zero. In field situations, plants typically operate at about
half the maximum rate of carbon gain (T). An approximately linear section of the
relationship between L and the typical point (T) has one NUE value (^C//`N).
Approaching the origin, NUE reaches the highest value (H); however, this condition is
associated with ahnormnllv work or tivina nl~ntc' ~ lthn,,
318
O R N L D W G 8 8 - 2 0 9 8
M
.
A
o
m
T/
a- -
H
o
i.
///l
// ~
// ALL
1/~,
!~
—d
NUTRIENT UPTAKE
Figure 1. Relationship between carbon gain and nutrient uptake where M and O are the
maximum and optimum carbon gain, TL is a linear range, and H is the highest nutrient-
use efficiency. See text for discussion of a, b, c, and d. A hypothesized natural
progression with increasing stand age is indicated by-- where canopy closure occurs at
point T.
_
uptake). If other
Nutrient-use efficiency can be a useful indicator of stress if the stress causes a
shift, such as Td, in the relationship (Fig. 1~. Perhaps such an effect could occur with
increases in ozone exposure (reducing carbon gain) and nitrogen deposition (increasing N
If other shifts in the relationship occur, such as Ta, Tb, and To, then NUE
would ne a poor indicator of stress. In two cases, change in nutrient uptake or carbon
gain (Ta or To, respectively) would be a better indicator of stress than NUE, whereas in
the case of Tb, NUE does not change and is completely insensitive as an indicator.
319
8
7
1 t,
~ v
a,
E 5
cot
o
~ 4
-
._
cot
-
c
3
In
o
o
s
~ 2
in
1
_
_
_
:
/o~
_ / 0
o
of
o/
o /
8/o
/
l
/
/
/
/
/
/
to/
/
0 10 20
30 40
Leat nitrogen (mg 9~' dry wt)
Figure 2. Light-saturated net photosynthesis rates of leaves of Eucalyptus species with differing
nitrogen concentration. Source: Reprinted with permission of Springer-Verlag N.Y., Inc. from
Oecologia, 1978. Copyright 1978 by Springer-Verlag.
320
EXAMPLES OF NUTRIENT-USE EFFICIENCY
Positive relationships have been demonstrated between light-saturated net photosynthesis and
foliar nitrogen concentration (Fig. 2) with occasional exceptions (Fig. 3~. In the latter case, the
relationship was positive between full-sun net photosynthesis of Pintos radiata and leaf phosphorus
but was negative for leaf nitrogen with the oldest needle age class generally having the lowest NUE
for both nitrogen and phosphorus. Short-term phytotoxic air pollutant exposure can reduce
photosynthesis (Reich and Amundson 1985), presumably reducing NUE since foliar nutrient levels
change at slower rates (Sheriff et al. 1986~. Monitoring of light-saturated leaf photosynthesis and
nutrient concentrations will provide valuable information on foliar functioning. In a scenario of
increasing ozone exposure and nitrogen deposition, a significant shift from the nonstressed
relationship between leaf photosynthesis and leaf nitrogen concentration may occur.
12
-
-
1
a,
-
w ~
_ ~
6
o
1
1
a
I'''
~ _. ,
0 0.4 0.8 1.2 0 4 8
N (g m~2)
P (8 me 2)
\
\
\
\
\
_ ~
b
~ .
12 16
Figure 3. Full-sun photosynthesis (Ama,,) of Pinus radiate needles in relation to leaf phosphorus
(P) and leaf nitrogen (N) for current needles ----, current + 1 year , and current + 2 year
..... (from Sheriff et al. 1986~.
321
Changes in NUE at the biochemical level are inferred for shifts to more energy-
efficient nitrogen nutrition. Pate (1986) theoretically calculated the costs of nitrogen (N)
assimilation in terms of adenosine triphosphate (ATP) required for various forms of N
relative to ATP needed for assimilation of ammonium. Symbiotic nitrogen fixation
required 16-29 mob ATP/mol NH4+, decreasing for NO3- assimilation (3-15 mol ATP/mol
NH4+) with the relative energy requirements for NH4+ assimilation being 1 mol ATP in
the Pate (1986) analysis. Nitrate assimilation in leaves was more efficient than root
assimilation due to linkage of nitrate reduction with photosynthesis. Foliar uptake of
nitric acid vapor is a more efficient N source (3 mol ATP/NH4+) than nitrate uptake into
roots (15 mol ATP/NH4+~.
The nitrogen-use efficiency of birch (Betula verrucosa) seedlings was shown to
decrease with increase in plant nitrogen concentration in the investigations of Ingestad
(1979~. Highest efficiency was obtained for the plants with lowest nitrogen concentration
(Fig. 4~. The relationship between net primary productivity (NPP) of aboveground
components and annual nitrogen uptake was shown by Miller ( 1984) to be linear (log-log
plot) for 39 stands (r2= o.go) that included coniferous and broadleaf forests from regions
that ranged from boreal to tropical (Fig. 5~. Since these data come from a wide range
of natural stress conditions, it is apparent that NUE is an insensitive measure of plant
response to stress. The nitrogen-use efficiency for aboveground tissues was about 170.
A linear relationship was also shown between NPP and annual phosphorus uptake but with
higher variability (r2= 0.74). The phosphorus-use efficiency for aboveground components
was about 17. Again, this value applied to a wide range of natural stress conditions
suggesting that the aboveground response of NUE to stress follows the trajectory Tb of
Fig. 1. -
Vitousek (1982) has suggested that for perennial vegetation, NUE is more
defined in terms of the organic matter loss (or storage) per unit of
(or storage). Monitoring of annual litterfall may thus provide an index of
NUE. The relationship between the inverse
total nitrogen in litterfall (Fig. 6) derived
appropriately
nutrient loss
aboveground NUE. The relationship between the inverse of litter nitrogen concentration
(NUE) and total nitrogen in litterfall (Fig. 6) derived for a wide range of forest
communities follows the pattern of Fig. 4, in which low abscissa values are associated
with high NUE. Given the rather wide scatter in the observations of Fig. 6, it may be
difficult to associate any change in litter NUE with a particular stress in a monitoring
program. There is much less variability if data for one species are considered, as shown
by the line segments in Fig. 6 for the fertilization study of Miller et al. (1976) with
Corsican pine (Pinus nigra). Determination of NUE on annual time scales restricts the
identification of particular stresses with the response since many stresses impact trees
during a year. Determination of NUE at shorter time steps is, however, not without
problems.
322
1 50
~ z 100
c
'
._ ~
.~' 3
i_
_
LU ~
50
o
. . _
_ ~
Optimum~
0 0.4 0.8
N. °/0 Fresh w!
Figure 4. Relationship of N-use efficiency to N status of birch (Betula verrucosa)
seedlings. Nitrogen status is measured as N percentage of seedling fresh weight. The
range in N status results from differing experimental N regimes (modified from Ingestad
1979~.
323
150
100
1a 50
~ 10
Be
0 ~
~ I
it'
~ 0
1
.
14
10
-
1a 6
s
~ 2
cam
. . . .
5 10 15 30
NPP, t t)a~1 yr-
· / -
· ~
~ ~ 0
o o
·o
ov ~
·'
.
. ,
·/
,, .
1
. . . ..
5 10 15 30
Figure S. Uptake of nitrogen and phosphorus into aboveground components as a function
of net primary production (NPP) using data reported for coniferous forests from boreal
), temperate ~ ), and tropical ~ ~ regions, and for broad-leaved forests from boreal ~ ),
temperate (0, Atnus rubra), and Mediterranean (~) regions. Uptake is calculated as
change in accumulation over time plus release in litterfall. Both regressions are
significant at P < 0.001, r2 values being 0.90 and 0.74 for N and P. respectively (from
Miller 1984~.
324
2 -
24C
J
tar 20C
5
0 16a
o
AS
2C
at
..
I,, 8C
fir
`3 4C
C
C
C C
\6C
\ C
C \
C C \
C Date D
M _44
C ~ D T T T
~ DNT
N N ~ N N
T Tr T ~T_~3
~ I I 1 1
20 ~ ~ ~ 1~ 120 140 1" 180 2=
~ IN LITTERfALL (KG HA-' YR-t )
Figure 6. The relationship between the amount of nitrogen in litterfall and the dry
mass to nitrogen ratio of that litterfall. Symbols are as follows: C= coniferous, D=
temperate deciduous, T= evergreen tropical, M= Mediterranean, N= temperate nitrogen
fixers. The line segments link data from a long-term fertilization study by Miller et al.
l 976) (from Vitousek l 982~.
NUE DURING THE ANNUAL CYCLE
Determination of AC/AN (NUE) during part of the growing season is a
straightforward harvesting and chemical analysis exercise involving substantial effort
when roots are included in a whole-plant measurement. Interpretation of the results as
NUE, however, is problematic due to phenological controls on growth, utilization of
internal carbon and nutrient storages, remobilization of nutrients, and the seasonality of
nutrient uptake (van den Driessche l 984~. Utilization of carbon and nutrient storage in
springtime foliar growth is initially "negative growth" because respiration exceeds carbon
gain. Shoot growth induces nutrient remobilization from adjacent leaf and twig tissues
325
and is essentially independent of nutrient uptake from soil (Titus and Kang 1982~; thus,
NUE of shoot growth is apparently infinite.
Many temperate forest species have deterministic leaf, twig, and flower growth (bud
control) and indeterminant stem thickening. Root growth tends to be indeterminant but
with periodic behavior due to reductions in root growth occurring during periods of shoot
growth (Bevington and Castle 1985~. Due to the asynchrony of shoot and root growth,
the same nutrient reserves can serve several functions during the growing season (Chapin
1980~. Fine-root (<1 mm diem) growth and mortality can be a large component of the
plant-carbon budget (Santantonio and Grace 1987), and the neglect of carbon allocation
to belowground processes in an aboveground determination of NUE greatly limits the
interpretation of this index as a stress indicator.
It is difficult to identify a time frame within the annual cycle in which
measurement of AC/AN can provide an unambiguous NUE indicator of plant response to
stress. Alternatively useful indicators based on carbon and nutrient dynamics may come
from consideration of these components in a whole-plant physiological framework that is
less constrained than the NUE concept.
CARBON-NUTRIENT RELATIONSHIPS
Foliar nutrient analysis (also soil chemical analysis) has been well established as a
means for identifying and monitoring nutrient deficiencies in plants. Diagnostic criteria
of nutrient stress (deficiency, toxicity) have been developed for a wide range of plants
(Chapman 1966, van den Driessche 1974), and these can provide useful guidance, although
retranslocation can mask deficiency in new foliage. Ozone exposure can result in
increases in foliar nutrient concentration in some cases. Skeffington and Roberts ( 1984)
showed increased Mg, K, and P concentrations in Pinus sylvestris needles exposed to
300 mg O~/m3 for 56 days but no effects from acid mist treatments. Decline in conifer
growth in southwestern West Germany has been associated with Mg and Ca deficiency
(Huttl and Wisniewski 1987) in needles and apparently rectified with fertilizer application.
Foliar analysis will continue to be a useful indicator of plant response to stress, and the
approach may be usefully extended by consideration of element ratios for elements with
differing retranslocation and storage dynamics (e.g., Ca immobile, N. P. K mobile in
leaves).
Cotrufo ( 1985) has evaluated several tissue analysis approaches as predictors of
loblolly pine response to nitrogen fertilization. Total N in xylem, total soluble N. and
arginine N of twigs and needles were greater in fertilized than in unfertilized trees.
Total needle N is not always a good indicator of tree N status (Ballard 1980, Sheriff et
al. 1986~; however, the reliability of alternative indicators is not well established.
Cotrufo ( 1985) noted that the interpretation of arginine N assays was complicated by
phosphorus nutrition and soil-water status, and xylem N of loblolly pine did not show a
strong relationship to N fertilization.
The relationship between starch and nitrogen content has been determined in birch
(Betula pendula) seedlings (McDonald et al. 1986) and in 30-year-old loblolly pine (Pinus
toeda) needles (Birk and Matson 1986~; both showed a similar pattern during the growth
period (Fig. 7, Fig. ~b), but the pine study conducted under field conditions showed much
more variability. Variability is likely to be a problem in interpretation of carbon-
nutrient relationships of tissues sampled from the field. During the dormant period
(February), the pattern of starch accumulation in relation to needle nitrogen was
reversed, with high starch levels being associated with high nitrogen levels (Fig. Sa).
326
-
1
3
C]
CR
250
ct 200
In
Cal
-
Q
is
e
go
100
is
In
z
.
150
50
.
\ -
·\
-
1,,.. 1
10 20 30 40
PLANT NITROGEN CONCENTRATION (me N 9 DW )
Figure 7. Steady-state dependence of plant starch concentration (ma starch g-1 dry
weight) on plant nitrogen concentration (ma N g- 1 dry weight) in seedling birch (from
McDonald et al. 1986).
~-
{D~
of
- ~
an
o
c)
m
Z
3
-
_
Cal
-
~ .
-
327
STARCH, mg/g
0 In 0 In 0 In 0
, . . .
o 1.
oo o o
o
pro 0
·~
o
0
0
·.
'
11 11
o
o
o
STARCH, mg/g
_ — ~ N
U' O ~ O
~ ' ~
~' 1l m
g 0 ~,
0
_
° 0 °
o Go
o
Motto
, ~ ~
o
o To
0
.
· ..
.
·
: ..
Figure S. Relationship between starch and nitrogen concentrations in loblolly pine
needles in control (open symbols) and fertilized (solid symbols) sites on the
coastal plain of South Carolina with a 30-year old pine stand for February (a) and June
(b) (from Birk and Matson 1986~.
CARBON AND NUTRIENT STORAGE
The principal soluble forms of nitrogen storage in woody plants are arginine, which
has a high N:C ratio, and asparagine (Titus and Kang 1982) with glutamine being
significant in some conifer species. Proteins are probably the most significant insoluble
nitrogen reserves in trees (van den Driessche 1984~. Phospholipids and "nonhydrolyzable
esters" were suggested as the main overwintering forms of phosphorus in cold-hardy
species (Chapin 1980, Chapin and Kedrowski 1983~. Sulfur can be stored in proteins,
328
amino acids, and sulfate forms (Linzon 1 97X). Potassium and inorganic phosphate
accumulate in vacuoles, and calcium is probably held in exchangeable form on cell walls,
particularly of xylem vessels. Starch is the dominant form of carbon storage, although
secondary compounds (terpenes, latex) can be significant carbon forms in some species.
Determination of the stored quantities of carbon and nutrients at the end of the growing
season could become a useful indicator of plant response to cumulative environmental
effects as well as of plant internal resources available for the next growing season.
Titus and Kang (1982) cite several examples where high levels of storage N are highly
correlated with new shoot growth of fruit trees during the following spring. Greater
knowledge of how to measure internal storage and how to interpret the values for forest
trees is needed before storage can be used as a definitive indicator. It is likely that not
all storage locations and forms are equally accessible. Perhaps leaf starch can be more
readily utilized by stem cambium than starch in ray cells of the stem. Further, the
concept of capacity defined as the change in storage per unit of chemical potential
energy (i.e., per unit biochemical driving force) may usefully distinguish between a range
of plant storage forms.
CHANGES IN CARBON-NUTRIENT RELATIONSHIPS WITH STAND AGE
Nutrient retranslocation from mature leaves to new leaves (Sheriff et al. 1986), from
twigs to new shoot growth, and from old roots to new roots (Titus and Kang 1982)
becomes increasingly important with time as a tree increases internal nutrient storage
relative to the annual growth demands. Miller ( 1984) noted that the relative demands
made by forests for soil minerals decrease markedly after canopy closure; trees
increasingly depend on internal retranslocation to meet nutrient requirements for annual
growth. Nitrogen retranslocation in a pine plantation was calculated to increase from 11
to 69 kg ha~1 year~1 with increase in age from 10 to 40 years. Similar stand age
changes were estimated for phosphorus and potassium. Meier et al. (1985) also estimated
an increased contribution of retranslocation in meeting the nutritional requirements of
aging Abies amabilis stands. Following canopy closure additional phytomass accumulates
largely as low-nutrient wood. This implies that with increasing stand age, NUE before
canopy closure is less than after canopy closure. A hypothesized progression of carbon
gain in relation to nutrient uptake with increasing stand age (Fig. 1 ) would give a range
of NUE values that may explain some of the variance in the data summarized by Miller
In leg. 3.
COMMENTS
Plants tend to operate within narrow ranges in the ratios of carbon to nutrients
and of nutrients to other nutrients (Chapin 1980, Garten 1976~. In the short term, plants
respond to stress with a change in physiological activity per unit tissue (leaf, root);
however, in the longer term, changes in leaf area and needle age classes (and, by
inference, fine-root turnover) are often significant signals of plant response to stress.
Continued stress, such as with high nitrogen deposition, can lead to physiological
imbalances. Mohren et al. ( 1986) identified large increases in N:P ratios in Douglas fir
needles in the Netherlands in recent times that were associated with phosphorus
deficiency. Nambiar (1987) evaluated the ratios of calcium (generally not retranslocated)
to other mobile nutrients (e.g., Ca:N, Ca:P, Ca:K) in fine-root and leaf tissues and
showed the relatively greater retranslocation of mobile nutrients from senescing leaves
than from old roots. It is possible that nutrient retranslocation from fine-roots may
only be significant in the zone close to the root tip with the effect being masked by
analysis of long lengths of root tissue. He also noted that prolonged drought had very
329
little effect on nutrient concentrations in fine-roots. Monitoring of tissue-nutrient
relationships can provide indications of stress impacts, although normal dynamics of
nutrient retranslocation and storage must be understood before abnormal signals can be
interpreted.
SUMMARY
NUE determined on annual time steps seems to be an insensitive indicator of stress
since changes in carbon gain and nutrient uptake tend to occur in the same
direction.
Determination of NUE within a growing period is complicated by deterministic
controls on growth, internal storage and retranslocation, and allocation to root
processes.
Light-saturated net photosynthesis generally increases with foliar nutrient (N. P)
concentration, and changes in this relationship may be a sensitive indicator of
short-term stress.
Identification of imbalances in the relationships between carbon and nutrient
dynamics of forest trees may lead to useful early warning indicators of stress
impacts, but this needs to be developed within a whole-plant physiological context.
ACKNOWLEDGMENT
Research sponsored! by the Carbon Dioxide Research Division, U.S. Department of
Energy under Contract No. DE-AC05-840R21400 with Martin Marietta Energy Systems,
Inc. Publication Number 3123, Environmental Sciences Division, Oak Ridge National
Laboratory, Oak Ridge, TN 37831.
REFERENCES
Ballard, R. 1980. Nitrogen fertilization of established loblolly pine stands: A flexible
silvicultural technique. Pp. 223-229 in Gen. Tech. Rept. S0-34, USDA Forest
Service, New Orleans.
Bevington~ K. B., and W. S. Castle. 1985. Annual root-growth pattern of young citrus
trees in relation to shoot growth, soil temperatures, and soil-water content. J. Am.
Soc. Hort. Sci. 110:840-845.
Birk, E. M., and P. A. Matson. 1986. Site fertility affects seasonal carbon reserves in
loblolly pine. Tree Physiol. 2:17-27.
Chapin, F. S. 1980. The mineral nutrition of wild plants. Ann. Rev. Ecol. Syst. 11:233-
260.
Chapin, F. S., and R. A. Kedrowski. 1983. Seasonal changes in nitrogen and phosphorus
fractions and autumn retranslocation in evergreen and deciduous Taiga trees.
Ecology 64:376-391.
330
Chapman, H. D. (ad.).
California, Riverside.
1966. Diagnostic criteria for plants and soils. University of
Cotrufo, C. 1985. Progress in tissue analysis to determine the response of loblolly pine
to nitrogen fertilization. Pp. 385-389 in Gen. Tech. Rept. S0-54, USDA Forest
Service, New Orleans.
Garten, C. T. 1976. Correlations between concentrations of elements in plants. Nature
261:686-688.
Huttl, R. F., and J. Wisniewski. 1987. Fertilization as a tool to mitigate forest decline
associated with nutrient deficiencies. Water Air Soil Poll. 33:265-276.
Ingestad, T. 1979. Nitrogen stress in birch seedlings. II. N. K, P. Ca, and Mg
nutrition. Physiol. Plant. 45: 149- 157.
Linzon, S. N. 1978. Effects of airborne sulfur pollutants on plants. Pp. 109- 162 in J.
O. Nriagu ted.), Sulfur in the Environment. II. Ecological Impacts. John Wiley and
Sons, New York.
McDonald, A. J. S., T. Lohammar, and A. Ericsson. 1986. Uptake of carbon and nitrogen
at decreased nutrient availability in small birch (Betula pendula Roth.) plants. Tree
Physiol. 2:61-71.
Meier, C. E., C. C. Grier, and D. W. Cole. 1985. Below- and aboveground N and P use
by Abies amabilis stands. Ecology 66:1928-1942.
Miller, H. G. 1984. Dynamics of nutrient cycling in plantation ecosystems. Pp. 53-78
in G. D. Bowen and E. K. S. Nambiar (eds.), Nutrition of Plantation Forests.
Academic Press, New York.
Miller, H. G., J. M. Cooper, and J. D. Miller. 1976. Effect of nitrogen supply on
nutrients in litterfall and crown leaching in a stand of Corsican pine. J. Appl. Ecol.
13:233-248.
Mohren, G. M. ]., J. van den Burg, and F. W. Burger. 1986. Phosphorus deficiency
induced by nitrogen input in Douglas fir in the Netherlands. Plant Soil 95:191-200.
Mooney, H. A., P. J. Ferrar, and R. O. Slatyer. 1978. Photosynthetic capacity and
carbon allocation patterns in diverse growth forms of Eucalyptus. Oecologia 36:103-
111.
Nambiar, E. K. S. 1987. Do nutrients retranslocate from fine roots? Can. J. For. Res.
17:913-918.
Pate, J. S. 1986. Economy of symbiotic nitrogen fixation. Pp. 299-325 in T. J. Givnish
(ed.), On the Economy of Plant Form and Function. Cambridge University Press,
New York.
Reich, P. B., and R. G. Amundson. 1985. Ambient levels of ozone reduce net
photosynthesis in tree and crop species. Science 230:566-570.
331
Santantonio, D., and J. C. Grace. 1987.
from biomass and decomposition data
1 7:900-908.
Estimating fine-root production and turnover
A compartment-flow model. Can. I. For. Res.
Sheriff, D. W., E. K. S. Nambiar, and D. N. Fife. 1986. Relationships between nutrient
status, carbon assimilation, and water-use efficiency in Pinus radiata (D. Don)
needles. Tree Physiol. 2:73-~.
Skeffington, R. A., and T. M. Roberts. 1984. The effects of ozone and acid mist on
Scots pine saplings. Report TPRD/L/2695/NS4, Central Electricity Generating Board,
Surrey, United Kingdom.
Titus, J. S., and S. M. Kang. 1982.
apple trees. Hort. Rev. 4:204-246.
Nitrogen metabolism, translocation, and recycling in
van den Driessche, R. 1974. Prediction of mineral nutrient status of trees by foliar
analysis. Bot. Rev. 40:347-394.
van den Driessche, R. 1984. Nutrient storage, retranslocation, and relationship of stress
to nutrition. Pp. 181-209 in G. D. Bowen and E. K. S. Nambiar (eds.), Nutrition of
Plantation Forests. Academic Press, New York.
Vitousek, P. 1982. Nutrient cycling and nutrient-use efficiency. Am. Nat. 119:553-572.
